International Journal of Microbiological Research 4 (3): 305-320, 2013
ISSN 2079-2093
© IDOSI Publications, 2013
DOI: 10.5829/idosi.ijmr.2013.4.3.81228
Microbial Bioremediation of Chromium in Tannery Effluent: A Review
P. Saranraj and D. Sujitha
Department of Microbiology, Annamalai University, Annamalai Nagar,
Chidambaram- 608 002, Tamil Nadu, India
Abstract: Chromium, a priority pollutant is well known for its mutagenicity, carcinogenicity and teratogenicity
in humans, experimental animals and plants. Extensive use of chromium in industries such as leather tanning,
stainless-steel production, electroplating and wood preservatives have resulted in chromium contaminated soil
and ground water at production sites which pose a serious threat to human health. Bioadsorption is the simple
uptake of the constituents of the effluent by the organisms without any usage in its metabolism. Biodegradation
means the breaking down of the constituents of the effluent into different fragments which will be either taken
as a substrate by the organisms or simply remain in the system i.e., metabolism of the constituents by the
organisms or simple cleavage by them into simpler fragments by the release of enzymes. Biodegradation is one
of the biological processes facilitating the chemical changes of pollutants by microorganisms present in the
polluted environment. Microorganisms are involved in the removal of toxic wastes, either in the environment
or in controlled treatment systems.
Key words: Tannery Effluent
Chromium
Bioremediation
INTRODUCTION
Tanning industries worldwide generate approximately
40 million waste containing chromium (Cr) every year.
With inadequate regulatory guidelines, wastes were
largely disposed on land and water odies throughout the
world. Studies showed that tannery waste disposals have
led to severe contamination of productive agricultural
land in Bangladesh, [3] in India [4] and in Australia [5].
Chromium is frequently one of the most toxic
elements present in tannery waste. High chromium
concentrations ranging from 1 to 50g/kg were reported in
soils surrounding tannery waste disposal sites in India,
with hexavalent chromium was present in groundwater at
these sites [6].
Chromium level was found to increase with increase
in the concentration of the tannery effluent. Chromium
associated pollution is of increasing concern nowadays.
Conventional methods for treatment of toxic chromate
include chemical reduction followed by precipitation, ion
exchange and adsorption on activated coal, alum, kaolinite
and ash which require large amounts of chemicals and
energy and therefore are unsuitable [7]. Several reports
have indicated biological reduction of hexavalent
chromium by microorganisms, both aerobes and
anaerobes. Biological reduction of hexavalent chromium
Elimination of heavy metals from industrial
wastewater is important for preserving the quality
of aquatic systems, streams and ground waters.
Contaminated waters are generally cleaned by
precipitation of a metallic oxyhydroxide sludge or by ion
exchange with synthetic resins. Various types of
nonliving biomass, bacteria, filamentous fungi, algae
and higher plants can be profitably used in alternative
metal removal processes because of their low cost and
the high ion exchange capacity of cell walls. The
hexavalent chromium compounds are comparatively
more toxic than trivalent chromium compounds due to
their higher solubility in water, rapid permeability
through biological membranes and subsequent interaction
with intracellular proteins and nucleic acids [1].
Accordingly, chromium and its compounds are placed
on the priority list of toxic chemicals by US EPA [2]. A
maximum acceptable concentration of 0.05 mg/l for
hexavalent chromium in drinking water has been
established on basis of health considerations. However,
its high toxicity, mutagenicity and carcinogenicity
renders it hazardous even at very low concentration.
Corresponding Author:
Bacteria and Fungi
P. Saranraj, Department of Microbiology, Annamalai University, Annamalai Nagar,
Chidambaram - 608 002, Tamil Nadu, India.
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usually occurs at a neutral pH range and generates an
insignificant quantity of chemical sludge as well as offers
potential cost – effective remediation strategy. A number
of chromium resistant microorganisms have been reported
to detoxify hexavalent chromium, which include
Pseudomonas sp., Microbacterium sp., Desulfovibrio sp.,
Enterobacter sp., Escherichia coli, Shewanella alga and
Bacillus sp., where the method of detoxification is
periplasmic biosorption, intracellular bioaccumulation and
biotransformation through direct enzymatic reaction or
indirectly with metabolites [8]. Some of the fungi that
remove chromium from tannery wastes are Aspergillus,
Nostoc and Cyanobacteria etc.
Biosorption by bacteria and fungi as an alternative
treatment option for wastewater containing heavy
metal has been reviewed by Kapoor and Viraghavan [9].
Any fungi can tolerate high concentration of potentially
toxic metals and with other microbes; this may
be correlated with decreased intracellular uptake or
impermeability. A close relation between toxicity and
intracellular uptake has been shown for Cu2+, Cd2+,
Co2+ and Zn2+ in yeast Saccharomyces cerevisiae.
Waste mycelia from industrial fermentation plants
(Aspergillus niger and Penicillium chrysogenum) were
used to as a biosorbent for removal of Zn ions from
aqueous environments, both batch wise as well as in
column mode. Under optimized conditions Aspergillus
niger and C. paspali were found superior to Penicillium
chrysogenum. Removal of lead ions from aqueous
solution by non-living biomass of Penicillium
chrysogenum was studied and observed that Pb2+ was
strongly affected by the pH in the range of 4-5.
Uptake of Pb2+ was 116 mg/g dry biomass, which was
higher than that of activated carbon and some other
microorganisms [10].
Chromium biosorption by non-living biomass of
Chlorella vulgaris, Clodophora crispate, Zoogloea
ramigera, Rhizopus arrhizus and Saccharomyces
cerevisiae was studied and observed that optimum
initial pH (1.0-2.0) of the metal ion solution affects the
metal uptake capacity of the biomass for all the
microorganisms. Maximum adsorption rates of metal ions
to microbial biomass were obtained at temperature in the
range of 25-35°C. The adsorption rates increased with
increasing the metal concentration of Chlorella vulgaris,
Clodophora crispate, Zoogloea ramigera, Rhizopus
arrhizus and Saccharomyces cerevisiae up to 200, 200, 75,
125 and 100 mg/l respectively [11]. Dead cells of
Saccharomyces cerevisiae removed 40% more uranium or
zinc than the corresponding live cultures.
Biosorptive capacity of different biosorbents
including dried mycelium of some species of fungi,
baggase, rice rusk and fermented baggase by selected
fungal species or natural micro flora was examined to
remove cyanide from industrial effluent. The biomass of
Rhizopus sexualis and the fermented baggase by
Rhizopus sexualis or Aspergillus terreus showed higher
sorption capacity than activated charcoal. The biomass of
Rhizopus sexualis and Mortierella ramanniana exhibited
higher CN sorptive capacity than ascomycetes e.g.
Aspergillus terreus and Penicillium capsulatum. Maximal
removal of Ni from electroplating industries occurred by
2.5 gm of biomass of Saccharomyces cerevisiae with in
5 hrs. Ni uptake capacity from aqueous solution was also
studied in filamentous fungi such as Rhizopus sp.,
Penicillium sp. and Aspergillus sp. The metal uptake was
highest by Rhizopus sp. [12].
Chromium: Chromium (Cr) is a transition metal present in
group VI-B of the periodic table. Although it can exist in
nine valence states, from -2 to +6 [13] only trivalent
chromium Cr (III) and hexavalent chromium Cr (VI) are
ecologically important because these are the most stable
oxidation states in the natural environment. Chromium is
a chemical element which has the symbol Cr and atomic
number 24. It is a steely gray, lustrous, hard metal
that takes a high polish and has a high melting point.
It is odorless, tasteless and malleable metal. The name of
the element is derived from the Greek word ‘chroma’
meaning color, because many of its compounds are
intensely colored. Chromium is an important metal due to
its high corrosion, resistance and hardness. It is used
extensively in manufacturing of stainless steel. Chromium
contamination of the environment is of concern because
of the mobility and toxicity of Cr (VI).
Trivalent and hexavalent chromium differ widely in
physicochemical properties and biological reactivity.
While Cr (VI) species and dichromate’s are extremely
water-soluble and mobile in the environment, Cr (III)
species are much less soluble and comparatively
immobile. Moreover, Cr (VI) is recognized to be highly
toxic, carcinogenic, mutagenic and teratogenic for
mammals including humans, whereas Cr (III) is an
essential trace element necessary for glucose, lipid and
amino-acid metabolism as well as a popular dietary
supplement [14].
Studies have revealed that Cr (VI) is approximately
100 times more toxic and 1000 times more mutagenic than
Cr (III). Although, trivalent chromium (Cr (III) or Cr3+) is
required in trace amounts for sugar and lipid metabolism
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in humans, however its deficiency causes disease.
Hexavalent chromium (Cr (VI) or Cr6+) is a toxin and a
carcinogen metal pollutant that tremendously affects the
environment at abandoned chromium production sites.
Hence its environmental cleanup is highly essential.
Cr (VI) is highly toxic, carcinogenic and mutagenic.
It causes severe diarrhea, ulcers, eye and skin
irritations, kidney dysfunction and probably lung
carcinoma. It is also associated with decrease in plant
growth and changes in plant morphology. Chromium is
present in the environment as either Chromium (III) or
Chromium (VI). Chromate [Cr (VI)] is highly soluble in
bacteria, it is transported rapidly across the cell
membranes via the sulfate pathway and reduced in the
cytoplasm to trivalent (III).Trivalent chromium, which
interacts with proteins and nucleic acids, however, is far
less soluble than hexavalent chromium and does not pass
through biological membranes [15].
Bacterial reduction has been found in metallic
minerals such as manganese, metal iron, mercury, selenite
and tellurite. Some microbial transformations enable the
bacteria to increase their tolerance toward toxic heavy
metals. Chromium, a transition metal, is one of the major
sources of environmental pollution. It is discharged into
the environment through the disposal of wastes from
industries like leather tanning, metallurgical and metal
finishing, textiles and ceramics, pigment and wood
preservatives, photographic sensitizer manufacturing
etc. [16].
In the environment chromium occurs mainly in
trivalent and hexavalent forms. The hexavalent chromium
(Cr6+) compounds are comparatively much more toxic than
those of trivalent chromium (Cr3+) [17]. There is only
limited investigation for mining effluent treatment
particularly Cr (VI) contaminants using microbial strains.
Till date there is no literature cited on any molecularly
identified and sequenced microbial species for chromium
resistant and removal from Sukinda region. Thus our
present study used potential indigenous microbial strains
for treatment of industrial and mining effluent that may be
suitable for biological treatment of Cr-contaminated
waste of Sukinda mines. This study a remediation route
for detoxification of Cr (VI) using an indigenous
microorganism.
engaged in the chrome tanning process. The tannery
waste primarily consists of chromium and protein.
Long term disposal of tannery wastes has resulted in
extensive contamination of agricultural land and water
sources in many parts of the India. There are more than
2500 tanneries in the country and nearly 80% of the
tanneries are engaged in the chrome tanning process.
In the process of tanning, chromium salts are used to
convert hide to leather and the waste water generated is
discharged into the environment which contains
chromium salts in the excess of the maximum permissible
limits. Tannery industry is one of the major industries in
India. In tannery effluent, Cr (VI) is present as either
dichromate (Cr2O72-) in acidic environment or as chromate
(CrO4-) in alkaline environments [18].
Heavy metals exhibit toxic effects on soil biota and
they can affect key microbial process and decrease
the number and activity of soil microorganisms [19].
Metal contaminants are commonly found in soils,
sediments and water. Metals pollutants can be produced
through industrial processes such as mining, refining and
electroplating. At low concentrations, metals can serve
as important components in life processes, often
serving important functions in enzyme productivity.
Metals can become toxic to many species. Fortunately,
microorganisms can affect the reactivity and mobility of
metals. Microorganisms that affect the reactivity and
mobility of metals can be used to detoxify some metals
and prevent further metals contamination. Thus far,
tolerance mechanisms for metals such as copper, zinc,
arsenic, chromium, cadmium and nickel have been
identified and described in detail.
When looking at the microbial communities of
metal-contaminated environments, it has been found
that among the bacteria present, there is more potential for
unique forms of respiration. Also, since the oxidation
state of a metal ion may determine its solubility, many
scientists have been trying to use microbes that are able
to oxidize or reduce heavy metals in order to remediate
metal-contaminated sites. Another implication of heavy
metal tolerance in the environment is that it may
contribute to the maintenance of antibiotic resistance
genes by increasing the selective pressure of the
environment. Calomiris et al. [20] studied bacteria isolated
from drinking water and found that a high percent of
bacteria that are tolerant to metals are also antibiotic
resistant.
Effluents from tannery, electroplating and electronic
industries contain chromium which is highly toxic.
This paper reported isolation of chromium tolerant
Bioremediation of Tannery Effluent by Using
Microorganisms: Tannery effluents are a major source of
aquatic pollution in India with chemical oxygen demand
(COD), biological oxygen demand (BOD) and hexavalent
chromium. Nearly 80% of the tanneries in India are
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microorganisms from solid waste as well as liquid effluent
of an electroplating industry. Nine isolates were obtained
that can tolerate chromium concentration up to 700 mg/L.
They reached their stationary phase within 8-12 hours
and can biosorbed 95% of initial 200 mg/L concentration
of chromium within 4-10 hours. Fourier Transform Infra
Red analysis of the biomass exposed to chromium
indicated that amino and carboxylate groups in the
biomass are involved in biosorption process. 16S RNA
results of two most active organisms indicate that they are
Bacillus marisflavi and Arthrobacter sp. and they show
98% and 96% homology similarity in the phylogenetic
tree, respectively [21].
Bento et al. [22] observed that maximum chromium
reduction occur at the optimum pH (7-9) and temperature
(30°C) of growth by Bacillus sp. Ravibabu [23] studied
the remediation of effluents using physical methods like
activated charcoal, pH ranges and time periods and
biological methods using the aquatic weed hyacinth as a
biological pollutant removal.
The pollution of the environment with toxic heavy
metals is spreading throughout the world along with
industrial progress. Microorganisms and microbial
products can be highly efficient bioaccumulations of
soluble and particulate forms of metals especially dilute
external solutions. Microbes related technologies may
provide an alternative or addition to conventional
method of metal removal or metal recovery. The present
study deals with isolation, identification and
characterization of heavy metal resistant bacteria was
isolated from tannery effluent collected in and around
Chennai, South India. Initially, a total of 50 isolates were
screened from tannery effluent [24].
Chromium, a transition metal, is one of the major
sources of environmental pollution. It is discharged into
the environment through the disposal of wastes from
industries like leather tanning, metallurgical and metal
finishing, textiles and ceramics, pigment and wood
preservatives, photographic sensitizer manufacturing etc.
In the environment chromium occurs mainly in trivalent
and hexavalent forms. The hexavalent chromium (Cr6+)
compounds are comparatively much more toxic than those
of trivalent chromium (Cr3+). The hexavalent chromium
compounds are comparatively more toxic than trivalent
chromium compounds due to their higher solubility in
water, rapid permeability through biological membranes
and subsequent interaction with intracellular proteins
and nucleic acids [25]. Accordingly, chromium and its
compounds are placed on the priority list of toxic
chemicals by US EPA [26]. A maximum acceptable
concentration of 0.05 mg/l for hexavalent chromium in
drinking water has been established on basis of health
considerations.
An Arthrobacter sp. and a Bacillus sp., isolated from
a long-term tannery waste contaminated soil, were
examined for their tolerance to hexavalent chromium
[Cr(VI)] and their ability to reduce Cr (VI) to Cr (III), a
detoxification process in cell suspensions and cell
extracts. Both bacteria tolerated Cr (VI) at 100 mg/ml on a
minimal salts agar medium supplemented with 0.5%
glucose, but only Arthrobacter could grow in liquid
medium at this concentration. Arthrobacter sp. could
reduce Cr (VI) upto 50 µg/ml, while Bacillus sp. was not
able to reduce Cr (VI) beyond 20 µg/ml. Arthrobacter
sp. was distinctly superior to the Bacillus sp. in terms of
their Cr (VI)-reducing ability and resistance to Cr (VI).
Assays with permeabilized (treated with toluene or
Triton X 100) cells and crude extracts demonstrated that
the Cr (VI) reduction was mainly associated with the
soluble protein fraction of the cell. Arthrobacter sp. has
a great potential for bioremediation of Cr (VI) containing
waste [27].
Cr (VI) (chromate) is a widespread environmental
contaminant. Bacterial chromate reductases can convert
soluble and toxic chromate to the insoluble and less toxic
Cr (III). Bioremediation can therefore be effective in
removing chromate from the environment, especially if the
bacterial propensity for such removal is enhanced by
genetic and biochemical engineering. Gram positive,
chromium (Cr)-resistant bacterial strain (ATCC 700729)
was isolated from effluent of tanneries. It was grown in
media containing potassium dichromate concentration up
to 80 mg ml 1 of the medium. The dichromate reducing
capability of the bacterium was checked by estimating the
amount of Cr (VI) in the medium before and after
introduction of bacterial culture. The influence of factors
like pH of the medium, concentration of Cr and the amount
of the inoculum was studied to determine the ability of
the bacterium to reduce Cr (VI) in the medium under
various conditions. In a medium containing dichromate
20 mg ml 1 more than 87% reduction of dichromate ions
was achieved within 72 hrs. The feasibility of the use of
this bacterial strain for detoxification of dichromate in the
industrial wastewater has been assessed. The isolated
strain can be exploited for specific environmental clean-up
operations [28].
Hexavalent chromium [Cr (VI)], is a toxic,
water-soluble contaminant present in many soils and
industrial effluents. Bacteria from various soils were
examined for Cr (VI) resistance and reducing potential.
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environment was discussed [35]. Turick et al. [36]
investigated several bacteria from various soils for
hexavalent chromium resistance and reducing potential.
Microbes selected from both hexavalent chromiumcontaminated and non-contaminated soils and sediments
were capable of catalyzing the reduction of hexavalent
chromium to trivalent chromium a less toxic, less
water-soluble form of chromium, demonstrating the utility
of using a selection strategy for indigenous hexavalent
chromium reducing bacteria in a bioprocess. As a result,
indigenous hexavalent chromium reducing microbes from
contaminated sites should provide the means for
developing a bioprocess to reduce hexavalent chromium
to trivalent chromium in non-sterile effluents such as
those from soil washes.
The occurrence of metal tolerant and antibiotic
resistant organisms was investigated in tannery effluent.
Seventy-seven isolates comprising heterotrophs and
coliforms which were tolerant to chromate level of >50µg/l
were selected for detailed study. The majority of the
coliforms were resistant to higher levels of chromate
(200 µg/ml) whereas around 3% of the heterotrophs were
resistant to Cr6+ at a level of >150 µg/l. All chromate
tolerant heterotrophs were also tolerant to Cu 2+ (100%)
whereas only 58.53% coliforms were tolerant to Cu 2+.
Except in the case of Cd2+ a higher number of heterotrophs
were found tolerant to other heavy metals tested. Both
groups of isolates were found sensitive to mercury.
Resistance to cephaloridine was more abundant
(P<0.001) in coliforms as compared to heterotrophs.
On the other hand a significantly higher number (P<0.01)
of heterotrophs showed resistance to streptomycin and
carbencillin. All coliforms were sensitive to
chloramphenicol. Around 80% and 31.70% of coliforms
and heterotrophs exhibited a relationship to the
combination of metals and antibiotics. Both heterotrophs
and coliforms tolerant to Hg2+ were also resistant to
polymixin-B [37].
Reduction of hexavalent chromium (chromate) to
less-toxic trivalent chromium was studied by using cell
suspensions and cell-free supernatant fluids from
Pseudomonas putida PRS2000. Chromate reductase
activity was associated with soluble protein and not with
the membrane fraction. The crude enzyme activity was
heat labile and showed a Km of 40, µM CrO42-. Neither
sulfate nor nitrate affected chromate reduction either
in vitro or with intact cells [38].
Bacterial strains (CrT-11, CrT-12, Brevibacterium sp.
CrT-13, CrT-14) were isolated from the effluents of
tanneries. All strains could resist very high concentration
Microbes selected from both Cr (VI)-contaminated and
non-contaminated soils and sediments were capable of
catalyzing the reduction of Cr (VI) to Cr(III) a less
toxic, less water-soluble form of Cr, demonstrating the
utility of using a selection strategy for indigenous
Cr(VI)-reducing bacteria in a bioprocess. As a result,
indigenous Cr (VI)-reducing microbes from contaminated
sites should provide the means for developing a
bioprocess to reduce Cr (VI) to Cr (III) in non-sterile
effluents such as those from soil washes. This approach
also avoids the contamination problems associated
with pure cultures of allochthonous microorganisms.
In addition the apparent ubiquity of Cr (VI)-reducing
bacteria in soil and sediments indicated the potential for
in situ bioremediation of Cr (VI)-contaminated soils and
ground water [29].
Viamajala et al. [30] studied the pollution effects of
tannery water and reported that the salts of the
tannery effluent percolates through the soil causing
severe salinity to the land. Srinath et al. [31] found
increased water soluble potassium, sulphur, iron,
ammonium acetate, extractable iron and soil sulphur as
well as traces of chromium in soils irrigated with tannery
effluent. Sultan and Hasnain [32] observed a reduction in
the micronutrient status with increasing concentrations
of tannery effluent in soil (incubated for six months).
The chromium level was also found to increase with
increase in the concentration of the tannery effluent.
Rajamani et al. [33] showed that chromates are absorbed
in soils and low pH favoured their reduction in soils.
Megharaj et al. [34] isolated chromium resistant
bacterial strain Bacillus cereus S-6 from effluents of
tannery which was used for the reduction of toxic
hexavalent chromium into less toxic trivalent chromium.
At an initial hexavalent chromium concentration of
100 µg/ml, the cytosol and membrane preparation of the
strain were able to reduce almost 67 and 43% of
hexavalent chromium within 24 hrs incubation period
while the heat killed cytosol and membrane preparation
reduced 24 and 18% within the same time period.
They reported that tannery effluent may change the
characteristics of soil and interfere with the intake of water
by plants. The presence of sulphide and chromium in
tannery effluent affects plant life and soil productivity.
Many genera of microbes like Bacillus, Enterobacter,
Escherichia, Pseudomonas and also some yeasts
and fungi help in bioremediation of metals and
chromium-contaminated soil and water by bioabsorption
and bioaccumulation of chromium. The potential of
bioremediation of metal toxicity and its impact on the
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become barren lands. Guha et al. [52] pointed out the
characteristics of tannery effluent led into the land and
said that the discharged effluents create severe land
pollution. Jonnalagadda et al. [53] studied the pollution
effects of tannery water and reported that the salts of the
tannery effluent percolates through the soil causing
severe salinity to the land. Komori et al. [54] assessed
that effluents containing toxic chemicals have seeped into
the arable land and agriculture has declined because of
the effects of tannery effluent. With the declined with in
productivity, the land value has also decreased. Lofroth
and Ames [55] found increased water soluble potassium,
sulphur, iron, ammonium acetate, extractable iron and soil
sulphur as well as traces of chromium in soils irrigated
with tannery effluent. Lovley and Phillips [56] showed
that the experimental and epidemiological evidence exists
for the carcinogenicity of some chromium compounds.
Therefore chromium has been designated as a priority
pollutant by US EPA.
Faisal and Hasnain [57] checked the multiple heavy
metals (Ni, Zn, Mn, Cu, Co, Pb) and antibiotic resistances
of Brevibacterium isolated from tannery effluents.
Thacker and Parikh [58] identified that the Brucella sp.
exhibit multiple heavy metals (Ni, Zn, Hg, Co, Pb)
tolerance and resistance to various antibiotics.
Middleton et al. [59] identified that Ochrobactrum tritici
is resistant to chromium, nickel, cobalt, cadmium and zinc
and able to grow in the presence of NaCl within the pH
range of 4 -10.
Obbard [60] observed a reduction in the micronutrient
status with increasing concentrations of tannery effluent
in soil (incubated for six months). The chromium level was
also found to increase with increase in the concentration
of the tannery effluent. Park et al. [61] showed that
chromates are absorbed in soils and low pH favoured their
reduction in soils. Pedersen [62] reported that tannery
effluent may change the characteristics of soil and
interfere with the intake of water by plants. The presence
of sulphide and chromium in tannery effluent affects plant
life and soil productivity.
of K2CrO4 that is upto 40 mg ml 1 on nutrient agar
and 25 mg ml 1 in nutrient broth. They have wide pH
(5 to 9) and temperature (24 to 42°C) growth range.
They exhibited multiple metals (Ni, Zn, Mn, Cu, Co and
Pb) and antibiotics (streptomycin, ampicillin, tetracycline,
kanamycin and chloramphenicol) resistances. All the
strains were able to reduce Cr (VI) in to Cr (III) aerobically.
Brevibacterium sp. CrT-13 accumulated and reduced more
Cr (VI) at all the concentrations applied in comparison to
the other strains. These bacterial strains also took up and
reduced Cr (VI) present in industrial effluents and their
reduction potential was not significantly affected in the
presence of different metallic salts [39].
Several reports have indicated biological reduction of
hexavalent chromium by microorganisms, both aerobes
and anaerobes. Biological reduction of hexavalent
chromium usually occurs at a neutral pH range and
generates an insignificant quantity of chemical sludge as
well as offers potential cost – effective remediation
strategy [40]. Subsequent studies have shown that the
capacity for hexavalent chromium reduction is widespread
and is reported in organisms such as Bacillus cereus,
Bacillus
subtilis,
Pseudomonas
aeruginosa,
Achromobacter, Eurydice, Micrococcus roseus and
Escherichia coli [41] as well as Pseudomonas ambigua
[42], Pseudomonas fluorescens [43], Enterobacter
cloacae [44], Streptomyces sp. [45], Pseudomonas putida
[46], D. desulfuricans and D. vulgaris [47] and
Pseudomonas liquefaciens [48].
Effect of Heavy Metals on the Growth of Bacteria:
As chromium metal ion is present abundantly in the
tannery effluents, the review in the present investigation
focuses primarily on effect of chromium on the growth of
bacteria. Germain and Patterson [49] inferred that
wastewaters containing hexavalent chromium (chromate)
are generated by many industries including the metal
finishing industry, leather tanning, petroleum refining,
textile manufacturing and pulp production. The chromium
present in industrial wastes is primarily in the hexavalent
form as chromate and dichromate. Petrilli and DeFlora [50]
found that the hexavalent chromium is highly soluble in
water while the reduced form of chromium, trivalent
chromium, forms less soluble chromium hydroxides under
non-acidic conditions. Hexavalent chromium is more toxic
than trivalent chromium and has been shown to be
mutagenic in a number of bacterial systems.
Flores and Perez [51] reported that about 800 acres of
agricultural land in Dindigul have been seriously
polluted by tannery effluents. All the fertile lands have
Chromium Adsorption by Bacteria: Srinath et al. [63]
studied that the Bacillus circulans and Bacillus
megaterium are able to bioaccumulate 34.5 and 32.0 mg
chromium/g dry weight, respectively and brought the
residual concentration of hexavalent chromium to the
permissible limit in 24 hrs when the initial concentration
was 50 mg hexavalent chromium/L. He stated that
biosorption of hexavalent chromium was shown by
Bacillus megaterium and another strain, Bacillus
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coagulans. Living and dead cells of Bacillus coagulans
biosorbed 23.8 and 39.9 mg chromium/g dry weight,
respectively, whereas, 15.7 and 30.7 mg chromium/g dry
weight was biosorbed by living and dead cells of
Bacillus megaterium, respectively.
Arvindhan and Madhan [64] assessed that the
reduction of hexavalent chromium by intact cells and a
cell-free extract of an actinomycete, Arthrobacter
crystallopoietes isolated from soil contaminated with
dichromate. Asatiani et al. [65] found that the
Arthrobacter sp. could reduce hexavalent chromium upto
50 mg/ml, while Bacillus sp. was not able to reduce
hexavalent chromium beyond 20 mg/ml. Arthrobacter
sp. was distinctly superior to the Bacillus sp. in terms of
their-hexavalent chromium reducing ability and resistance
to hexavalent chromium. Assays with permeabilized
(treated with toluene or Triton X 100) cells and crude
extracts demonstrated that the reduction of hexavalent
chromium is mainly associated with the soluble protein
fraction of the cell.
Muhammed Faisal and Shahida Hasnain [66]
demonstrated that the ability of Brevibacterium cells to
accumulate toxic hexavalent chromium at different
chromate concentrations (100, 500 and 1000 µg/ml) in
different time intervals (15 min, 2 hours and 4 hours).
They showed that the Arthrobacter oxydans does a
complete uptake of hexavalent chromium concentration
(35 mg/ml) in about 10 days.
Gonul Donmez and Nur Kocberber [67] isolated
the microorganisms and their hexavalent chromium
bioaccumulation capacities increased by enrichment
procedure. At the end of the experiments, the highest
specific chromium uptake was obtained at pH 8 as
109.45mgg 1 for 164.4mgl 1 initial hexavalent chromium
concentration in the absence of NaCl. In the highest
NaCl concentration the maximum specific chromium
uptake was found at pH 9 (26.2mgg 1) in samples with
lower initial hexavalent chromium concentrations at pH 7
(as 87.5mgg 1) for high initial hexavalent chromium
concentrations.
Baldi et al. [68] studied the biosorption process for
treatment of electroplating wastewater containing
hexavalent chromium. They also explained that to treat
chromium wastewaters is through the use of biomaterials
as a low-cost adsorbent for chromium. Various
biomaterials, such as dead biomass (of microalgae,
seaweed, fungi and bacteria), agricultural waste biomass,
industrial waste biomass and biomaterial-based
containing activated carbons for the removal of
chromium from aqueous solutions or wastewaters in a
batch or column reactor system.
Rao et al. [69] investigated that the adsorption of
hexavalent chromium ions from aqueous solutions on
crude tamarind fruit shell, HCl treated and Oxalic acid
treated shells at room temperatures The influence of
different experimental parameters such as pH, effect of
initial metal ion concentration and effect of dosage of
adsorbent on biosorption were evaluated.
Chromium Adsorption by Fungi: Chromium and nickel
are released into the environment by a large number of
processes such as electroplating, leather tanning, wood
preservation, pulp processing, steel manufacturing, etc.
and the concentration levels of chromium and nickel in the
environment widely varies. These two metals are of major
concern because of their larger usages in developing
countries and their non degradability nature. Hexavalent
chromium is highly soluble in water and carcinogenic to
human. Ni(II) is more toxic and carcinogenic metal when
compared with Ni(IV). Due to their toxic effects on living
systems stringent limits have been stipulated for the
discharge of chromium and nickel into the environment.
According to ISI: Bureau of Indian Standard (BIS) the
industrial effluent permissible discharge level of
Cr(VI) and Ni(II) into inland water is 0.1 and 3.0 mg
L 1, respectively. Gupta et al. [70] tested the tolerance
and accumulation of hexavalent chromium by marine
seaweed associated strains of Aspergillus flavus and
Aspergillus niger. They revealed that both the isolates
accumulated more than 25% of the chromium supplied.
Aspergillus flavus invariably exhibited higher
accumulation potential.
Igwe and Abia [71] found that the chromium was
bioremoved from tannery industries effluent by
Aspergillus oryzae. Aspergillus oryzae can grow in
different concentration of chromium 120-1080 mg/L.
They observed that maximum biomass growth and
chromium removal rate at pH, 3.3, trivalent chromium
concentration equal to 240 mg/L and inoculum size equal
to 0.12% (dry weight) were 0.25 (dry weight ) and 94.2%,
respectively. They stated that bacterial strains were
isolated and enriched from the contaminated site of
Tamil Nadu Chromates and Chemicals Limited (TCCL)
premises, Ranipet, Tamil Nadu, India. It was found that
a bacterial concentration of 15+/-1.0 mg/g of soil
(wet weight) 50 mg of molasses/g of soil as carbon source
were required for the maximum hexavalent chromium
reduction. The bioreactor operated at these conditions
could reduce entire hexavalent chromium (5.6 mg /g of
soil) in 20 days.
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Intl. J. Microbiol. Res., 4 (3): 305-320, 2013
Srivastava and Thakur [72] explained the potency of
Aspergillus niger evaluated in shake flask culture
by absorption of chromium at pH 6, temperature 30°C.
He inoculated Aspergillus niger in soil microcosm
(40% moisture content) with different concentrations of
chromate (250, 500, 1000, 1500 and 2000ppm), it removed
more than 70% chromium in soil contaminated by 250 and
500ppm of chromate. However, chromium-contaminated
soil (2000ppm of potassium chromate) mixed with compost
(5% and 10%) significantly removed chromium in
presence of fungus, Aspergillus niger.
Igwe and Abia [73] explained about the sorption
behavior of some biosorbents with various heavy metals,
their relative performance evaluated and a bioseperation
process flow diagram for heavy metal removal from
wastewater using biosorbents was proposed. Some
biosorbents such as algae, fungi, bacteria have been
investigated for their capacity towards heavy metals.
environments. It provides the means for developing a
bioprocess to reduce hexavalent chromium to trivalent
chromium in non sterile effluents. This approach also
avoids the contamination problems associated with pure
cultures of allochthonous microorganisms. Kankal [80]
added easily degradable organic substances of a very
narrow C:N ratio and found marked hexavalent chromium
reduction. Kapoor and Viraraghavan [81] investigated
several bacteria from various soils for hexavalent
chromium resistance and reducing potential. Microbes
selected from both hexavalent chromium-contaminated
and non contaminated soils and sediments were capable
of catalyzing the reduction of hexavalent chromium to
trivalent chromium a less toxic, less water-soluble form of
chromium, demonstrating the utility of using a selection
strategy for indigenous hexavalent chromium reducing
bacteria in a bioprocess. As a result, indigenous
hexavalent chromium reducing microbes from
contaminated sites should provide the means for
developing a bioprocess to reduce hexavalent chromium
to trivalent chromium in non-sterile effluents such as
those from soil washes.
Kapoor and Viraraghavan [82] reported that the
reduction of hexavalent chromium to trivalent chromium
decreases the toxicity and mobility of chromium
contaminants in soils and water. In addition, the formation
of a highly insoluble trivalent chromium product would
decrease the likelihood o f future trivalent chromium
re-oxidation. Kapoor et al. [83] reported that chromium
reduction by Pseudomonas putida. He explained the
characterization of chromate reductase activities by a
soluble protein fraction from Pseudomonas putida.
Chromate reduction required either NADH or NADPH for
maximum activity. Romanenko and Koren Ken [84]
indicated that the early investigations demonstrate the
facultative anaerobic bacteria such as Pseudomonas
dechromaticans, Pseudomonas chromatophila and
Aeromonas dechromatica remove hexavalent chromium
from solution by the formation of a trivalent chromium
precipitate.
Romanenko and Korenken [85] first reported that the
Aeromonas sp. Capable of hexavalent chromium reduction
>70% anaerobically. He also found that several facultative
anaerobes tolerant to high levels of chromate (>400µg/ml)
were isolated from tannery effluents. Laxman and More
(2001) [86] found that chromate is a oxidizing agent that
is reduced intracellularly to pentavalent chromium
and reacts with nucleic acids and other cell components
to produce mutagenic and carcinogenic effects on
Chromium Reduction by Bacteria: Many industrial
sites are contaminated with toxic trace metals which are
then diverted into the environment, leading to pollution of
surface and groundwater supplies. Heavy metals have
a wide range of industrial applications such as
electroplating, metal finishing or tanning and in mining
industries. As a result, they are present in many industrial
discharges. These heavy metals pose serious
environmental implications as they remain mobilized in the
food chain and are toxic to the biota [74]. Komori et al.
[75] inferred that conventional methods for removing toxic
chromium include chemical reduction followed by
precipitation, ion exchange and adsorption on activated
coal, alum, kaolinite and ash. However, most of these
methods require high energy or large quantities of
chemical reagents.
Jeyasingh and Philip [76] indicated that vast
literature is available on chromate reduction by bacteria
including physiological, biochemical and genetic
aspects of chromate toxicity/resistance and reduction.
Juliette Lamberta and Mohammed Rakib [77] explained
that reduction of hexavalent chromium by the earthworm
Eisenia foetida. He also suggested that Eisenia foetida
play an important role during occasional hexavalent
chromium pollution of soils. Kader et al. [78] explained
that the technical process for removing trivalent chromium
from tannery wastewater via precipitation.
Kamaludeen et al. [79] demonstrated that isolation
of hexavalent chromium reducing anaerobes from
hexavalent chromium contaminated and non contaminated
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Intl. J. Microbiol. Res., 4 (3): 305-320, 2013
biological
systems.
LilianaMorales-Barrera
and
EliseoCristiani-Urbina [87] assessed that hexavalent
chromium reduction to pentavalent chromium is
responsible for chromate toxicity, further reduction to
trivalent chromium leads to the formation of stable, less
soluble and less toxic trivalent chromium. Reduction of
hexavalent chromium to trivalent chromium is therefore a
potentially useful process for remediation of hexavalent
chromium affected environments.
Luef et al. [88] observed the microbial reduction of
toxic hexavalent chromium has practical importance,
because biological strategies provide green technology
that is cost-effective. Mahvi et al. [89] inferred that the
recovery of chromium III from tannery wastewater by
using three aqueous oxidants, Hydrogen peroxide,
Sodium Hypochlorite and Calcium Hypochlorite were
independently oxidizing to soluble chromate under
alkaline conditions. Megharaj and Naidu [90] highlighted
that amino acid mixtures are the best electron donars for
hexavalent chromium reduction. Infact, in one study,
the number of viable cells decreased in the initial stages
after hexavalent chromium was added and 50% of the
added hexavalent chromium was reduced before viable
cell numbers increased over what was present prior to
hexavalent chromium addition. Modak et al. [91] stated
that organic
matter content and bioactivity were
important factors in reducing almost 96% of the added
hexavalent chromium under aerobic, field moist
conditions. It suggests that organic amended soils can
readily reduce hexavalent chromium and could promote
excellent removal efficiency.
Rathinam Aravindhan et al. [92] demonstrated that
the biological removal of carcinogenic hexavalent
chromium using mixed Pseudomonas strains. Under
optimal conditions, 100mg/L of hexavalent chromium was
completely reduced within 180 min. Puranik and
Paknikar [93] found that the hexavalent chromium was
reduced by gram negative bacteria Providencia sp.
It reduced chromate to 100% at a concentration ranging
from 100-300 mg/L. It also exhibited multiple heavy metal
tolerance. Quintelas and Fernandes [94] assessed that
the low temperature reduction of hexavalent chromium
by a Arthrobacter aurescens.
Urvashi Thacker and Rasesh Parikh [95] assessed
that the reduction of chromate by cell-free extract of
Brucella sp. Isolated from hexavalent chromium
contaminated sites. High hexavalent
chromium
concentration resistance and high hexavalent chromium
reducing ability of the strain make it a suitable candidate
for bioremediation. Shaili Srivastava and Indu Shekhar
Thakur [96] studied the relationship between the
hexavalent chromium resistance of the culturable microbial
community and the hexavalent chromium resistance and
reducing ability strains of each population. Shaili
Srivastava and Indu Shekhar Thakur [97] isolated
chromium resistant bacterial strain Bacillus cereus S-6
from effluents of tannery was used for the reduction of
toxic hexavalent chromium into less toxic trivalent
chromium. At an initial hexavalent chromium
concentration of 100 µg/mL, the cytosol and membrane
preparation of the strain were able to reduce almost 67 and
43% of hexavalent chromium within 24 hrs incubation
period while the heat killed cytosol and membrane
preparation reduced 24 and 18% within the same time
period.
Shikha Rastogi and Saxene [98] concluded that
Pseudomonas fluorescens LB 300, reduces hexavalent
chromium while growing aerobically glucose medium, also
grows in an anaerobic chamber containing oxygen-free
nitrogen on agar plates containing acetate as a potential
electron donor and hexavalent chromium as the potential
electron acceptor. However, no hexavalent chromium
reduction occurs in anaerobic liquid cultures. Siegel et al.
[99] demonstrated that Enterobacter cloacae strain HO1
reduces hexavalent chromium while growing under
anaerobic conditions in a medium that contains acetate
and amino acids as a potential electron donars.
Enterobacter cloacae can grow anaerobically in the
absence of added hexavalent chromium and no evidence
for hexavalent chromium depended growth has been
presented.
Srinath et al. [100] found that some organism reduce
hexavalent chromium during anaerobic growth in media in
which hexavalent chromium is provided as the sole
electron acceptor, in no instance has hexavalent chromium
reduction definitely been shown to yield energy to
support anaerobic growth. For example, Pseudomonas
chromatophila uses hexavalent chromium as an electron
acceptor to support growth under anaerobic conditions
with a variety of electron donars, including the
non-fermentable substrate, acetate.
Saranraj et al. [101] isolated a bacterial strain from
tannery effluent and identified it as Enterococcus
casseliflavus. It showed a high level resistance of
800 µg/ml chromium. The minimal inhibitory concentration
of chromium was found to be 512 µg/ml of potassium
dichromate in Nutrient broth medium. The chromium
adsorption was more significant by the live cells than
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Intl. J. Microbiol. Res., 4 (3): 305-320, 2013
Properties of the Tannery Effluents: Bioremediation has
developed from the laboratory to a fully commercialized
technology over the last 30 years in many industrialized
countries. A successful bioremediation scheme relies on
the management of soil microbial populations capable of
catabolizing the contaminants. Heavy metals exhibit toxic
effects on soil biota and they can affect key microbial
processes and decrease the number and activity of soil
microorganisms [114]. Microbial population has often
been proposed to be an easy and sensitive indicator of
anthropogenic effects on soil ecology. Cr (VI) has been
reported to cause shifts in the composition of soil
microbial populations and known to cause detrimental
effects on microbial cell metabolism at high
concentrations. Quite a few studies on soil contamination
of heavy metal from industrial sites were reported [115].
Since, the discovery of the first microbe capable
of reducing Cr6+ in the 1970s [116], the search for
Cr6+-reducing microorganisms (both aerobic and
anaerobic) has been enthusiastically pursued, with
numerous strains being isolated. Based on recent
isolation and purification of Cr6+ reductases from aerobic
bacteria and the fact that the process involved in
Cr6+ reduction occurring under anaerobic conditions is
starting to be understood, biological processes for
treating chromium contaminated sites are becoming very
promising. Some of the emerging technologies for the
mitigation and remediation of Cr (VI) include microbial
strategies for in situ and on-site bioremediation strategies
and use in permeable reactive barriers.
Discovery of microorganisms capable of reducing
Cr (VI) to Cr (III) have significant potential in development
of in situ or on-site bioremediation strategies. In 1977, the
first reported bacterial strains, Pseudomonas, were
isolated from chromate (CrO42- contaminated sewage
sludge by Russian scientists N.A. Romanenko and
V. Korenkov. Since 1977, several other CrO42- reducing
strains have been reported, including other strains such
as B. cereus, B. subtilis, P. aeruginosa, P. ambigua,
P. fluorescens, E. coli, Achromobacter eurydice,
Micrococcus
roseus,
Enterobacter
cloacae,
Desulfovibrio desulfuricans and D. vulgaris [117].
A number of bacteria in other genera, viz., Bacillus spp.,
E. coli ATCC 33456, Shewanella alga BrY-MT and a
few unidentified strains have also been shown to reduce
Cr6+ [118]. Terry Beveridge [119] worked on isolation and
characterization of a chromium reducing bacterium from a
chromated copper arsenate contaminated site. Reports
conclude a Gram-negative bacterium (CRB5) isolated from
killed cells at different time intervals. It was observed
that, the inoculation of Enterococcus casseliflavus
reduced the BOD and COD values of tannery effluent.
The maximum adsorption of chromium was at a
temperature of 35 to 45°C and at a pH of 7.0 to 7.5.
Subsequent studies have shown that the capacity for
hexavalent chromium reduction is widespread and is
reported in organisms such as Bacillus cereus, Bacillus
subtilis, Pseudomonas aeruginosa, Achromobacter
Eurydice, Micrococcus roseus and Escherichia coli
[102] as well as Pseudomonas ambigua [103],
Pseudomonas fluorescens [104], Enterobacter cloacae
[105], Streptomyces sp. [106], Pseudomonas putida [107],
Desulfovibrio desulfuricans and Desulfovibrio vulgaris
[108] and Pseudomonas liquefaciens [109].
Chromium Reduction by Fungi: Filamentous fungi can
be profitably used in processes for heavy metals removal
from wastewater due to their low cost and to the high ion
exchange capacity of their cell walls. This property arises
from the large density of functional groups present in the
cell wall (carboxyl, hydroxyl, amine, phosphoryl,
sulfhydryl), creating a negatively charged surface [110].
The sorption properties of cell have been widely
studied by solution chemistry [111], but the chemical
nature of complexing groups is not known. The nature of
Pb binding sites on the cell walls of the filamentous
fungus Penicillium chrysogenum was investigated at the
macroscopic level by sorption isotherm and at the
molecular level by extended X-ray absorption free
structure (EXAFS) spectroscopy by varying the
metal concentration by two orders of magnitude, down
to 4.8 10.3 m mol Ph/g.
ShailiSrivastava and InduShekharThakur [112]
isolated the Aspergillus niger from soil and effluent of
leather tanning mills had higher activity to remove
chromium. He also indicated that removal of more than
75% chromium by Aspergillus niger determined by
diphenylcarbazide colorimetric assay and atomic
absorption spectrophotometry after 7 days.
LilianaMorales-Barrera and EliseoCristiani-Urbina
[113] identified that hexavalent chromium was removed
by a Trichoderma inhamatum fungal strain isolated from
Tannery effluent. And the fungus exhibited a remarkable
capacity to tolerate and completely reduced hexavalent
chromium concentrations up to 2.43mM. He indicated that
the Trichoderma inhamatum fungal strain may have
potential applications in bioremediation of hexavalent
chromium contaminated wastewaters.
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Intl. J. Microbiol. Res., 4 (3): 305-320, 2013
a chromium-contaminated site that was capable of
reducing hexavalent chromium to an insoluble precipitate,
thereby removing this toxic chromium species from
solution.
Laxman and More [120] found that the effect of
pH and temperature on maximum chromium reduction
occurred in pH range of 6-7 and 37°C -50°C by
Streptomyces griseus. Zainul Akmar Zakaria et al. [121]
observed that maximum chromium reduction occur at the
optimum pH (7 – 9) and temperature (30°C) of growth by
Bacillus sp. Ravibabu [122] studied the remediation of
effluents using physical methods like activated charcoal,
pH ranges and time periods and biological methods using
the aquatic weed hyacinth as a biological pollutant
removal.
Yoshinobu Ishibashi and Simon Silver [123] explained
about the various industrial discharges of toxic chemical
pollutants requires biological treatment. He showed a
permissible reduction of BOD (80%-90%) for both paper
mill and dying industry effluents. Duangporn Kantachote
et al. [124] identified the reduction of biological oxygen
demand in tannery effluents from 4967 mg/L to 1010 mg/ml
after inoculation of Rhodopseudomonas blastica. He also
found the reduction of chemical oxygen demand from
7328 mg/L to 3371 mg/L in tannery effluents.
Young Hak Kwak and Han Bok Kim [125]
demonstrated that the maximum amount of biomass
growth and chromium removal rate occurred at pH 5 and
were 0.35% (Dry weight) and 96.6%, respectively. And the
enzymatic activities of Aspergillus oryzae at pH 5 was
very suitable in which the living cell of fungi were able to
grow significantly. He also observed that the maximum
biomass growth and chromium removal rate was
achieved at 30°C and were 0.29% (Dry weight) and
96.9%, respectively. While decreasing temperature below
24°C decreased fungal growth and enzymatic activity.
Furthermore, increasing the temperature up to about 40°C,
decreased the fungal growth and consequently the
chromium removal extent.
Abubacker and Ramanathan [126] found that another
approach was molecular techniques used to genetically
engineer plants that could hyperaccumulate chromium
and other heavy metals. In a recent study, it was found
that there was a high correlation in chromium content in
shoots of many plant species with the content of other
heavy metals such as cadmium, copper, nickel and zinc.
He stated that accumulations of these heavy metals in
plant shoots were found to be associated. Using recent
molecular approaches, it will be possible to evolve plants
suitable for phytoremediation of soils and waters
contaminated with chromium and other heavy metals.
Jonnalagadda Raghava Rao [127] reported biological
removal of carcinogenic chromium (VI) using mixed
Pseudomonas strains. In this study an aerobic reduction
of Cr (VI) to Cr (III) by employing mixed Pseudomonas
cultures isolated from a marshy land has been reported.
The role of chromium concentration, temperature, pH and
additives on the microbial reduction of Cr (VI) has been
investigated. NADH was found to enhance the rate of
reduction of Cr (VI). Complete reduction of Cr (VI) has
been possible even at Cr (VI) concentrations of 300 ppm.
Sadeeshkumar et al. [128] studied that the removal of
COD from tannery wastewater is attractive for the
betterment of environment. Tanning wastewater
containing high COD (3413 mg/ml) was oxidized with
aqueous oxidants i.e. Hydrogen peroxide, Sodium
Hypochlorite and Calcium Hypochlorite at different
temperatures and reaction durations.
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